Beyond the one-locus-one-miRNA paradigm: microRNA isoforms enable deeper insights into breast cancer heterogeneity

Nucleic Acids Research

Volumn 43, Issue 19, 2015, Pages 9158-9175

  Telonis, Aristeidis G ^a   Loher, Phillipe ^a   Jing, Yi ^a   Londin, Eric ^a   Rigoutsos, Isidore ^a  

^a THOMAS JEFFERSON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MICRORNA; MICRORNA 183 5P; TRANSCRIPTOME; UNCLASSIFIED DRUG; ARGONAUTE PROTEIN; RNA ISOFORM; RNA PRECURSOR;

ARTICLE; BREAST CANCER; CAUCASIAN; CONTROLLED STUDY; DOWN REGULATION; FEMALE; HUMAN; HUMAN TISSUE; MICROARRAY ANALYSIS; PHENOTYPE; PRIORITY JOURNAL; RACE DIFFERENCE; RNA SEQUENCE; TRANSCRIPTION REGULATION; UPREGULATION; BREAST; BREAST TUMOR; ETHNOLOGY; GENE EXPRESSION REGULATION; GENE LOCUS; GENETIC VARIATION; GENETICS; METABOLISM; TUMOR CELL LINE;

ARGONAUTE PROTEINS; BREAST; BREAST NEOPLASMS; CELL LINE, TUMOR; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; GENETIC LOCI; GENETIC VARIATION; HUMANS; MICRORNAS; RNA ISOFORMS; RNA PRECURSORS; TRANSCRIPTOME;

EID: 84959377931     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkv922     Document Type: Article

References (88)

1. DeSantis,C., Ma,J., Bryan,L. and Jemal,A. (2014) Breast cancer statistics, 2013. CA: Cancer J. Clin., 64, 52-62.
2. Thakkar,J.P. and Mehta,D.G. (2011) A review of an unfavorable subset of breast cancer: estrogen receptor positive progesterone receptor negative. Oncologist, 16, 276-285.
3. Dawson,S.J., Provenzano,E. and Caldas,C. (2009) Triple negative breast cancers: clinical and prognostic implications. Eur. J. Cancer, 45(Suppl. 1), 27-40.
4. Huang,B., Warner,M. and Gustafsson,J.A. (2014) Estrogen receptors in breast carcinogenesis and endocrine therapy. Mol. Cell. Endocrinol., doi:10.1016/j.mce.2014.11.015.
5. Jordan,V.C. and Brodie,A.M. (2007) Development and evolution of therapies targeted to the estrogen receptor for the treatment and prevention of breast cancer. Steroids, 72, 7-25.
6. Vici,P., Pizzuti,L., Natoli,C., Gamucci,T., Di Lauro,L., Barba,M., Sergi,D., Botti,C., Michelotti,A., Moscetti,L. et al. (2015) Triple positive breast cancer: A distinct subtype? Cancer Treat. Rev., 41, 69-76.
7. Ademuyiwa,F.O., Edge,S.B., Erwin,D.O., Orom,H., Ambrosone,C.B. and Underwood,W. 3rd (2011) Breast cancer racial disparities: unanswered questions. Cancer Res., 71, 640-644.
8. Cancer Genome Atlas, N. (2012) Comprehensive molecular portraits of human breast tumours. Nature, 490, 61-70.
9. Carey,L.A., Perou,C.M., Livasy,C.A., Dressler,L.G., Cowan,D., Conway,K., Karaca,G., Troester,M.A., Tse,C.K., Edmiston,S. et al. (2006) Race, breast cancer subtypes, and survival in the Carolina Breast Cancer Study. JAMA, 295, 2492-2502.
10. Dietze,E.C., Sistrunk,C., Miranda-Carboni,G., O'Regan,R. and Seewaldt,V.L. (2015) Triple-negative breast cancer in African-American women: disparities versus biology. Nat. Rev. Cancer, 14, 248-254.
11. Sorlie,T. (2007) Molecular classification of breast tumors: toward improved diagnostics and treatments. Methods Mol. Biol., 360, 91-114.
12. Sorlie,T., Perou,C.M., Tibshirani,R., Aas,T., Geisler,S., Johnsen,H., Hastie,T., Eisen,M.B., van de Rijn,M., Jeffrey,S.S. et al. (2001) Gene expression patterns of breast carcinomas distinguish tumor subclasses with clinical implications. Proc. Natl. Acad. Sci. U.S.A., 98, 10869-10874.
13. Prat,A. and Perou,C.M. (2011) Deconstructing the molecular portraits of breast cancer. Mol. Oncol., 5, 5-23.
14. Parker,J.S., Mullins,M., Cheang,M.C., Leung,S., Voduc,D., Vickery,T., Davies,S., Fauron,C., He,X., Hu,Z. et al. (2009) Supervised risk predictor of breast cancer based on intrinsic subtypes. J. Clin. Oncol., 27, 1160-1167.
15. Badve,S., Dabbs,D.J., Schnitt,S.J., Baehner,F.L., Decker,T., Eusebi,V., Fox,S.B., Ichihara,S., Jacquemier,J., Lakhani,S.R. et al. (2011) Basal-like and triple-negative breast cancers: a critical review with an emphasis on the implications for pathologists and oncologists. Mod. Pathol., 24, 157-167.
16. Dawson,S.J., Rueda,O.M., Aparicio,S. and Caldas,C. (2013) A new genome-driven integrated classification of breast cancer and its implications. EMBO J., 32, 617-628.
17. Eroles,P., Tormo,E., Pineda,B., Espin,E. and Lluch,A. (2015) MicroRNAs in breast cancer: one More Turn in Regulation. Curr. Drug Targets, 16.
18. Kusenda,B., Mraz,M., Mayer,J. and Pospisilova,S. (2006) MicroRNA biogenesis, functionality and cancer relevance. Biomed. Pap. Med. Fac. Univ. Palacky Olomouc Czech. Repub., 150, 205-215.
19. Hata,A. and Lieberman,J. (2015) Dysregulation of microRNA biogenesis and gene silencing in cancer. Sci. Signal., 8, re3.
20. Bartel,D.P. (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell, 116, 281-297.
21. Winter,J., Jung,S., Keller,S., Gregory,R.I. and Diederichs,S. (2009) Many roads to maturity: microRNA biogenesis pathways and their regulation. Nat. Cell Biol., 11, 228-234.
22. Bartel,D.P. (2009) MicroRNAs: target recognition and regulatory functions. Cell, 136, 215-233.
23. Schirle,N.T., Sheu-Gruttadauria,J. and MacRae,I.J. (2014) Structural basis for microRNA targeting. Science, 346, 608-613.
24. Iorio,M.V., Ferracin,M., Liu,C.G., Veronese,A., Spizzo,R., Sabbioni,S., Magri,E., Pedriali,M., Fabbri,M., Campiglio,M. et al. (2005) MicroRNA gene expression deregulation in human breast cancer. Cancer Res., 65, 7065-7070.
25. Berindan-Neagoe,I. and Calin,G.A. (2014) Molecular pathways: microRNAs, cancer cells, and microenvironment. Clin. Cancer Res., 20, 6247-6253.
26. Di Leva,G., Garofalo,M. and Croce,C.M. (2014) MicroRNAs in cancer. Annu. Rev. Pathol., 9, 287-314.
27. López-Camarillo,C.s. and Marchat,L.A. (2013) MicroRNAs in cancer. CRC Press/Taylor & Francis Group, Boca Raton.
28. Mogilyansky,E. and Rigoutsos,I. (2013) The miR-17/92 cluster: a comprehensive update on its genomics, genetics, functions and increasingly important and numerous roles in health and disease. Cell Death Differ., 20, 1603-1614.
29. Kozomara,A. and Griffiths-Jones,S. (2011) miRBase: integrating microRNA annotation and deep-sequencing data. Nucleic Acids Res., 39, D152-D157.
30. Loher,P., Londin,E.R. and Rigoutsos,I. (2014) IsomiR Expression Profiles in Human Lymphoblastoid Cell Lines Exhibit Population and Gender Dependencies. Oncotarget, 5, 8790-8802.
31. Vickers,K.C., Sethupathy,P., Baran-Gale,J. and Remaley,A.T. (2013) Complexity of microRNA function and the role of isomiRs in lipid homeostasis. J. Lipid Res., 54, 1182-1191.
32. Guo,L. and Chen,F. (2014) A challenge for miRNA: multiple isomiRs in miRNAomics. Gene, 544, 1-7.
33. Tan,G.C., Chan,E., Molnar,A., Sarkar,R., Alexieva,D., Isa,I.M., Robinson,S., Zhang,S., Ellis,P., Langford,C.F. et al. (2014) 5′ isomiR variation is of functional and evolutionary importance. Nucleic Acids Res., 42, 9424-9435.
34. Pillai,M.M., Gillen,A.E., Yamamoto,T.M., Kline,E., Brown,J., Flory,K., Hesselberth,J.R. and Kabos,P. (2014) HITS-CLIP reveals key regulators of nuclear receptor signaling in breast cancer. Breast Cancer Res. Treat., 146, 85-97.
35. Londin,E., Loher,P., Telonis,A.G., Quann,K., Clark,P., Jing,Y., Hatzimichael,E., Kirino,Y., Honda,S., Lally,M. et al. (2015) Analysis of 13 cell types reveals evidence for the expression of numerous novel primate- and tissue-specific microRNAs. Proc. Natl. Acad. Sci. U.S.A., 112, E1106-E1115.
36. Flicek,P., Amode,M.R., Barrell,D., Beal,K., Billis,K., Brent,S., Carvalho-Silva,D., Clapham,P., Coates,G., Fitzgerald,S. et al. (2014) Ensembl 2014. Nucleic Acids Res., 42, D749-D755.
37. Core Team,R (2014) R: A language and environment for statistical computing. R Found. Stat. Comput. Vienna. Austria, http://www.R-project.org/.
38. Hui,W., Gel,Y.R. and Gastwirth,J.L. (2008) lawstat: An R Package for Law, Public Policy and Biostatistics. J. Stat. Softw., 28, 1-26.
39. Lucas,A. (2014) amap: Another Multidimensional Analysis Package. R Package Version 0.8-14, http://CRAN.R-project.org/package=amap.
40. Sanchez,G. (2013) DiscriMiner: Tools of the Trade for Discriminant Analysis. R Package Version 0.1-29, http://CRAN.R-project.org/package=DiscriMiner.
41. Tusher,V.G., Tibshirani,R. and Chu,G. (2001) Significance analysis of microarrays applied to the ionizing radiation response. Proc. Natl. Acad. Sci. U.S.A., 98, 5116-5121.
42. Chen,H. and Boutros,P.C. (2011) VennDiagram: a package for the generation of highly-customizable Venn and Euler diagrams in R. BMC Bioinformatics, 12, 35.
43. Galili,T. (2014) dendextend: Extending R's dendrogram functionality. R Package Version 0.18.3., http://CRAN.R-project.org/package=dendextend.
44. Quackenbush,J. (2001) Computational analysis of microarray data. Nat. Rev. Genet., 2, 418-427.
45. Barker,M. and Rayens,W. (2003) Partial least squares for discrimination. J. Chemometrics, 17, 166-173.
46. Huang da,W., Sherman,B.T. and Lempicki,R.A. (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc., 4, 44-57.
47. Huang da,W., Sherman,B.T. and Lempicki,R.A. (2009) Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res., 37, 1-13.
48. Miranda,K.C., Huynh,T., Tay,Y., Ang,Y.S., Tam,W.L., Thomson,A.M., Lim,B. and Rigoutsos,I. (2006) A pattern-based method for the identification of MicroRNA binding sites and their corresponding heteroduplexes. Cell, 126, 1203-1217.
49. Cline,M.S., Smoot,M., Cerami,E., Kuchinsky,A., Landys,N., Workman,C., Christmas,R., Avila-Campilo,I., Creech,M., Gross,B. et al. (2007) Integration of biological networks and gene expression data using Cytoscape. Nat. Protoc., 2, 2366-2382.
50. Yancy,H.F., Mason,J.A., Peters,S., Thompson,C.E. 3rd,Littleton,G.K., Jett,M. and Day,A.A. (2007) Metastatic progression and gene expression between breast cancer cell lines from African American and Caucasian women. J. Carcinog., 6,8.
51. Mungall,A.J., Palmer,S.A., Sims,S.K., Edwards,C.A., Ashurst,J.L., Wilming,L., Jones,M.C., Horton,R., Hunt,S.E., Scott,C.E. et al. (2003) The DNA sequence and analysis of human chromosome 6. Nature, 425, 805-811.
52. Kriegel,A.J., Liu,Y., Fang,Y., Ding,X. and Liang,M. (2012) The miR-29 family: genomics, cell biology, and relevance to renal and cardiovascular injury. Physiol. Genomics, 44, 237-244.
53. Slusarz,A. and Pulakat,L. (2015) The two faces of miR-29. J. Cardiovas. Med., 16, 480-490.
54. Chaulk,S.G., Thede,G.L., Kent,O.A., Xu,Z., Gesner,E.M., Veldhoen,R.A., Khanna,S.K., Goping,I.S., MacMillan,A.M., Mendell,J.T. et al. (2011) Role of pri-miRNA tertiary structure in miR-17-92 miRNA biogenesis. RNA Biol., 8, 1105-1114.
55. Chaulk,S.G., Xu,Z., Glover,M.J. and Fahlman,R.P. (2014) MicroRNA miR-92a-1 biogenesis and mRNA targeting is modulated by a tertiary contact within the miR-17-92 microRNA cluster. Nucleic Acids Res., 42, 5234-5244.
56. Clark,P.M., Loher,P., Quann,K., Brody,J., Londin,E.R. and Rigoutsos,I. (2014) Argonaute CLIP-Seq reveals miRNA targetome diversity across tissue types. Sci. Rep., 4, 5947.
57. Rigoutsos,I. and Tsirigos,A. (2010) In:Slack,F (ed).MicroRNAs in Development and Cancer. Imperial College Press, pp. 237-259.
58. Xia,Z., Clark,P., Huynh,T., Loher,P., Zhao,Y., Chen,H.W., Ren,P., Rigoutsos,I. and Zhou,R. (2012) Molecular dynamics simulations of Ago silencing complexes reveal a large repertoire of admissible 'seed-less' targets. Sci. Rep., 2, 569.
59. Li,P., Sheng,C., Huang,L., Zhang,H., Huang,L., Cheng,Z. and Zhu,Q. (2014) MiR-183/-96/-182 cluster is up-regulated in most breast cancers and increases cell proliferation and migration. Breast Cancer Res., 16, 473.
60. Ueno,K., Hirata,H., Shahryari,V., Deng,G., Tanaka,Y., Tabatabai,Z.L., Hinoda,Y. and Dahiya,R. (2013) microRNA-183 is an oncogene targeting Dkk-3 and SMAD4 in prostate cancer. Br. J. Cancer, 108, 1659-1667.
61. Dambal,S., Shah,M., Mihelich,B. and Nonn,L. (2015) The microRNA-183 cluster: the family that plays together stays together. Nucleic Acids Res., 43, 7173-7188.
62. Bussing,I., Slack,F.J. and Grosshans,H. (2008) let-7 microRNAs in development, stem cells and cancer. Trends Mol. Med., 14, 400-409.
63. Cloonan,N., Wani,S., Xu,Q., Gu,J., Lea,K., Heater,S., Barbacioru,C., Steptoe,A.L., Martin,H.C., Nourbakhsh,E. et al. (2011) MicroRNAs and their isomiRs function cooperatively to target common biological pathways. Genome Biol., 12, R126.
64. Starega-Roslan,J., Koscianska,E., Kozlowski,P. and Krzyzosiak,W.J. (2011) The role of the precursor structure in the biogenesis of microRNA. Cell. Mol. Life Sci., 68, 2859-2871.
65. Koppers-Lalic,D., Hackenberg,M., Bijnsdorp,I.V., van Eijndhoven,M.A., Sadek,P., Sie,D., Zini,N., Middeldorp,J.M., Ylstra,B., de Menezes,R.X. et al. (2014) Nontemplated nucleotide additions distinguish the small RNA composition in cells from exosomes. Cell Rep., 8, 1649-1658.
66. Hwang,H.W., Wentzel,E.A. and Mendell,J.T. (2007) A hexanucleotide element directs microRNA nuclear import. Science, 315, 97-100.
67. Biagioni,F., Bossel Ben-Moshe,N., Fontemaggi,G., Yarden,Y., Domany,E. and Blandino,G. (2013) The locus of microRNA-10b: a critical target for breast cancer insurgence and dissemination. Cell Cycle, 12, 2371-2375.
68. Chen,J. and Wang,X. (2014) MicroRNA-21 in breast cancer: diagnostic and prognostic potential. Clin. Transl. Oncol., 16, 225-233.
69. Cheng,Z., Cui,W., Ding,Y., Liu,T., Liu,W., Qin,Y., Xia,W., Xu,J., Zhang,Y. and Zou,X. (2014) BMP8B mediates the survival of pancreatic cancer cells and regulates the progression of pancreatic cancer. Oncol. Rep., 32, 1861-1866.
70. Mima,K., Fukagawa,T., Kurashige,J., Takano,Y., Uchi,R., Ueo,H., Matsumura,T., Ishibashi,M., Sawada,G., Takahashi,Y. et al. (2013) Gene expression of bone morphogenic protein 8B in the primary site, peripheral blood and bone marrow of patients with gastric cancer. Oncol. Lett., 6, 387-392.
71. Lehmann,T.P., Korski,K., Ibbs,M., Zawierucha,P., Grodecka-Gazdecka,S. and Jagodzinski,P.P. (2013) rs12976445 variant in the pri-miR-125a correlates with a lower level of hsa-miR-125a and ERBB2 overexpression in breast cancer patients. Oncol. Lett., 5, 569-573.
72. Donatelli,S.S., Zhou,J.M., Gilvary,D.L., Eksioglu,E.A., Chen,X., Cress,W.D., Haura,E.B., Schabath,M.B., Coppola,D., Wei,S. et al. (2014) TGF-beta-inducible microRNA-183 silences tumor-associated natural killer cells. Proc. Natl. Acad. Sci. U.S.A., 111, 4203-4208.
73. Li,X., Kroin,J.S., Kc,R., Gibson,G., Chen,D., Corbett,G.T., Pahan,K., Fayyaz,S., Kim,J.S., van Wijnen,A.J. et al. (2013) Altered spinal microRNA-146a and the microRNA-183 cluster contribute to osteoarthritic pain in knee joints. J. Bone Miner. Res., 28, 2512-2522.
74. Rizos,E., Siafakas,N., Koumarianou,A., Katsantoni,E., Filippopoulou,A., Ntounas,P., Touloumis,C., Kastania,A. and Zoumpourlis,V. (2012) miR-183 as a molecular and protective biomarker for cancer in schizophrenic subjects. Oncol. Rep., 28, 2200-2204.
75. Chang,Y.Y., Kuo,W.H., Hung,J.H., Lee,C.Y., Lee,Y.H., Chang,Y.C., Lin,W.C., Shen,C.Y., Huang,C.S., Hsieh,F.J. et al. (2015) Deregulated microRNAs in triple-negative breast cancer revealed by deep sequencing. Mol. Cancer, 14, 36.
76. Lowery,A.J., Miller,N., Dwyer,R.M. and Kerin,M.J. (2010) Dysregulated miR-183 inhibits migration in breast cancer cells. BMC Cancer, 10, 502.
77. Li,J., Fu,H., Xu,C., Tie,Y., Xing,R., Zhu,J., Qin,Y., Sun,Z. and Zheng,X. (2010) miR-183 inhibits TGF-beta1-induced apoptosis by downregulation of PDCD4 expression in human hepatocellular carcinoma cells. BMC Cancer, 10, 354.
78. Zhou,H. and Rigoutsos,I. (2014) MiR-103a-3p targets the 5′ UTR of GPRC5A in pancreatic cells. RNA, 20, 1431-1439.
79. Zhou,H. and Rigoutsos,I. (2014) The emerging roles of GPRC5A in diseases. Oncoscience, 1, 765-776.
80. Masuda,H., Zhang,D., Bartholomeusz,C., Doihara,H., Hortobagyi,G.N. and Ueno,N.T. (2012) Role of epidermal growth factor receptor in breast cancer. Breast Cancer Res. Treat., 136, 331-345.
81. Samatar,A.A. and Poulikakos,P.I. (2014) Targeting RAS-ERK signalling in cancer: promises and challenges. Nat. Rev. Drug Discov., 13, 928-942.
82. Hartman,Z.C., Poage,G.M., den Hollander,P., Tsimelzon,A., Hill,J., Panupinthu,N., Zhang,Y., Mazumdar,A., Hilsenbeck,S.G., Mills,G.B. et al. (2013) Growth of triple-negative breast cancer cells relies upon coordinate autocrine expression of the proinflammatory cytokines IL-6 and IL-8. Cancer Res., 73, 3470-3480.
83. Ades,F., Zardavas,D., Bozovic-Spasojevic,I., Pugliano,L., Fumagalli,D., de Azambuja,E., Viale,G., Sotiriou,C. and Piccart,M. (2014) Luminal B breast cancer: molecular characterization, clinical management, and future perspectives. J. Clin. Oncol., 32, 2794-2803.
84. Finlay-Schultz,J., Cittelly,D.M., Hendricks,P., Patel,P., Kabos,P., Jacobsen,B.M., Richer,J.K. and Sartorius,C.A. (2014) Progesterone downregulation of miR-141 contributes to expansion of stem-like breast cancer cells through maintenance of progesterone receptor and Stat5a. Oncogene, 34, 3676-3687.
85. Le,M.T., Hamar,P., Guo,C., Basar,E., Perdigao-Henriques,R., Balaj,L. and Lieberman,J. (2014) miR-200-containing extracellular vesicles promote breast cancer cell metastasis. J. Clin. Invest., 124, 5109-5128.
86. Tuomarila,M., Luostari,K., Soini,Y., Kataja,V., Kosma,V.M. and Mannermaa,A. (2014) Overexpression of microRNA-200c predicts poor outcome in patients with PR-negative breast cancer. PloS One, 9, e109508.
87. Berezikov,E. (2011) Evolution of microRNA diversity and regulation in animals. Nat. Rev. Genet., 12, 846-860.
88. Wheeler,B.M., Heimberg,A.M., Moy,V.N., Sperling,E.A., Holstein,T.W., Heber,S. and Peterson,K.J. (2009) The deep evolution of metazoan microRNAs. Evol. Dev., 11, 50-68.